Mammary olfactory signalisation in females and odor processing in neonates: ways evolved by rabbits and humans.

Mammalian females have long been known to release olfactory attraction in their offspring. Mammary odor cues control infant state, attention and directional responses, delay distress responses, stimulate breathing and positive oral actions, and finally can boost learning. Here, we survey female-offspring odor communication in two mammalian species - European rabbits and humans - taken as representatives of evolutionary extremes in terms of structure and dynamics of mother-infant relations, and level of neonatal autonomy. Despite these early psychobiological differences, females in both species have evolved mammary structures combining multiple sources of endogenous and exogenous odorants, and of greasy fixatives, conferring on them a chemocommunicative function. To process these mammary chemosignals, neonates have co-evolved multiple perceptual mechanisms. Their behaviour appears to be driven by plastic mechanism(s) calibrated by circumstantial odor experience in preceding and current environments (fetal and postnatal induction of sensory processes and learning), and by predisposed mechanisms supported by pathways that may be hard-wired to detect species-specific signals. In rabbit neonates, predisposed and plastic mechanisms are working inclusively. In human neonates, only plastic mechanisms could be demonstrated so far. These mammary signals and cues confer success in offspring's approach and exploration of maternal body surface, and ensuing effective initial feeds and rapid learning of maternal identity. Although the duration of the impact of these mammary signals is variable in newborns of species exposed to contrasting life-history patterns, their functional role in setting on infant-mother interaction in the context of milk transfer can be crucial.

A pheromone that rapidly promotes learning in the newborn.

Mammalian neonates depend on their mother's food supply and use a defined sequence of actions to find her mammary area. Their behavior is initially uncertain and demanding but rapidly becomes optimal. Efficient learning is thus operating in newborns. For instance, European rabbit (Oryctolagus cuniculus) pups localize the nipples through typical orocephalic movements. These movements are released by the mammary pheromone secreted in milk or by prenatally learned odor cues. During daily nursing, they also learn odors associated with the mother, supposedly with sucking as the main reinforcer. We here investigate the role of the mammary pheromone as an enforcer of early olfactory learning in newborn rabbits. In testing more than 950 pups, we show that the mammary pheromone promotes learning of neutral odorants paired with the pheromone in single and short trials. The pheromone-induced learning is efficient from birth and supports successive acquisition of distinct odorants. This reveals that a mammalian pheromone can function as a "cognitive organizer" that promotes early learning of relevant environmental cues.

Rabbit pup response to the mammary pheromone: from automatism to prandial control.

Rabbit pups display nipple-search behavior in response to maternal odor cues such as the Mammary Pheromone (MP). Here, we assessed in 3 steps whether the activity of the MP is influenced by prandial and/or rhythmic factors during early development. To address this point, the activity of the MP was tested in 690 pups varying in age (day 0, 2, 5 or 10), prandial state (sucked or un-nursed) and period of their 24-h cycle (-6 to +12 h after the daily sucking). In Experiment 1, the responsiveness of d0 pups was high and stable during the whole day, whether they are nursed or deprived of sucking. The MP activity was thus unaffected by colostrum ingestion. Experiment 2 revealed that some differences appear the next days: whereas the responsiveness of d2 pups was also very high during the 24-h cycle (>94%), it decreased in d5-d10 pups immediately after sucking (<48%), with a rapid recuperation in d5 pups. Experiment 3 showed that this postprandial drop in response to the MP disappeared in d5-d10 pups that missed the daily nursing, suggesting that it resulted from post-ingestive/post-absorptive events rather than from rhythm activity-related factors. Taken together, the results show a progressive change in the circadian dynamics of the MP-induced orocephalic response as a function of age modulated by prandial state. This indicates a transition from an automatic response to the MP to a response regulated by physiological factors associated with satiation.